Microbial sensitivity to temperature and sulfate deposition modulates greenhouse gas emissions from peat soils

Abstract

Peatlands are among the largest natural sources of atmospheric methane (CH 4 ) worldwide. Microbial processes play a key role in regulating CH 4 emissions from peatland ecosystems, yet the complex interplay between soil substrates and microbial communities in controlling CH 4 emissions as a function of global change remains unclear.Herein, we performed an integrated analysis of multi-omics data sets to provide a comprehensive understanding of the molecular processes driving changes in greenhouse gas (GHG) emissions in peatland ecosystems with increasing temperature and sulfate deposition in a laboratory incubation study. We sought to first investigate how increasing temperatures (4, 21, and 35°C) impact soil microbiome-metabolome interactions; then explore the competition between methanogens and sulfate-reducing bacteria (SRBs) with increasing sulfate concentrations at the optimum temperature for methanogenesis. Our results revealed that peat soil organic matter degradation, mediated by biotic and potentially abiotic processes, is the main driver of the increase in CO 2 production with temperature. In contrast, the decrease in CH 4 production at 35°C was linked to the absence of syntrophic communities and the potential inhibitory effect of phenols on methanogens. Elevated temperatures further induced the microbial communities to develop high growth yield and stress tolerator trait-based strategies leading to a shift in their composition and function. On the other hand, SRBs were able to outcompete methanogens in the presence of non-limiting sulfate concentrations at 21°C, thereby reducing CH 4 emissions. At higher sulfate concentrations, however, the prevalence of communities capable of producing sufficient lowmolecular-weight carbon substrates for the coexistence of SRBs and methanogens was translated into elevated CH 4 emissions. The use of omics in this study enhanced our understanding of the structure and interactions among microbes with the abiotic components of the system that can be useful for mitigating GHG emissions from peatland ecosystems in the face of global change.

Unravelling substrate availability and redox interactions on methane production in peat soils of China

“…The SO 4 2− concentration (1000 μM) in Phase I was much higher than the need for sulphate reducers (Blodau & Moore, 2003), but the addition of SO 4 2− in our experiment promoted the release of DOC and methanogenesis (Figure 3). Our results are in agreement with the result found by Dettling et al (2006); CH 4 emission was stimulated by an increase of SO 4 2− concentration in the presence of sufficient OM, and producing adequate low‐molecular‐weight C substrates with the coexistence of sulphate reducing bacteria (SRBs), and methanogens at high sulphate concentrations (5 mM) reducing CH 4 suppression (AminiTabrizi et al, 2023).…”

“…For instance, Dalcin Martins et al (2017) reported that the Prairie Pothole Region (North America) wetlands with large labile carbon pools (DOC ~180 mg C L −1 ), potentially mitigating competitive inhibition of CH 4 production by sulphate‐reducing bacteria through mechanisms like providing noncompetitive substrates such as methanol. A recent laboratory incubation experiment by AminiTabrizi et al (2023) suggests that the competition between SRBs and methanogens in the presence of low sulphate concentrations (0.75 mM) can reduce CH 4 emissions, but at high sulphate concentrations (5 mM), and increased low‐molecular carbon substrates can promote coexistence of SRBs and methanogens, thereby increasing CH 4 emissions. Thus, it is inferred that with sufficient C substrate and appropriate EAs concentration in peat soils, the increase of labile carbon utilization caused by the addition of EAs is greater than the inhibition of EAs on methanogenesis, attenuating the suppression of CH 4 production.…”

“…While previous research suggested that elevated Fe(III) and SO 4 2− inhibit CH 4 production in wetland soils (Yu et al, 2016), recent evidence indicates that dissolved organic matter (DOM) acts as a primary driver of methanogenesis in peatlands (Hopple et al, 2019). Any restrictions on SOC can affect CH 4 formation (Baldwin & Mitchell, 2012; Palareti et al, 2017) as the addition of SO 4 2− in soil promotes CH 4 emissions with sufficient carbon substrates (AminiTabrizi et al, 2023; Dettling et al, 2006). Similarly, Yan and Zhou (2019) demonstrated that ferrihydrite promoted microbial activity during periods of organic carbon limitation and further stimulated CH 4 emission by 26.4% in peatland soil.…”

“…Currently, research suggests that the existing Redox Ladder Theory controlling methane production processes has limitations, with potential overlap or intersection in the reduction processes of EAs (AminiTabrizi et al, 2023). Simultaneously, a more in‐depth exploration is required to understand the impact of EAs on methane oxidation processes in peat soils.…”

Temperature sensitivity of organic carbon decomposition in lake sediments is mediated by chemodiversity

“…Our results indicated that $$$ {R}_{{\mathrm{CO}}_2} $$$ in lake ecosystems was mainly regulated by sediment properties, such as pH, carbon quantity and quality (e.g., chemodiversity). $$$ {R}_{{\mathrm{CO}}_2} $$$ was promoted at lower pH (Figure 2a), likely because the lower pH facilitates acid‐catalyzed organic carbon decomposition (AminiTabrizi et al., 2023), as well as the release or dissolution of mineral‐protected organic matter (Ding et al., 2020; Groeneveld et al., 2020). $$$ {R}_{{\mathrm{CO}}_2} $$$ was greater in the organic carbon rich sediments (Figure 2a; Figure S7a), which was consistent with results from riverine (Comer‐Warner et al., 2018; Stegen et al., 2023) and terrestrial forest ecosystems (Li et al., 2020).…”